Bioactive Compounds of Edible Purple Laver Porphyra sp. (Nori)

Review Cite This: J. Agric. Food Chem. 2017, 65, 10685−10692

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Bioactive Compounds of Edible Purple Laver Porphyra sp. (Nori) Tomohiro Bito,† Fei Teng,‡ and Fumio Watanabe*,† †

Department of Agricultural, Life and Environmental Sciences, Faculty of Agriculture, Tottori University, Tottori 680-8553, Japan Department of Food Quality and Safety, College of Food Science, Northeast Agricultural University, Harbin 150030, China

‡

ABSTRACT: Porphyra sp. (nori) is widely cultivated as an important marine crop. Dried nori contains numerous nutrients, including vitamin B12, which is the only vitamin absent from plant-derived food sources. Vegetarian diets are low in iron and vitamin B12; depletion of both causes severe anemia. Nori also contains large amounts of iron compared with other plant-derived foods and eicosapentaenoic acid, which is an important fatty acid found in fish oils. In nori, there are also many bioactive compounds that exhibit various pharmacological activities, such as immunomodulation, anticancer, antihyperlipidemic, and antioxidative activities, indicating that consumption of nori is beneficial to human health. However, Porphyra sp. contains toxic metals (arsenic and cadmiun) and/or amphipod allergens, the levels of which vary significantly among nori products. Further evidence from human studies of such beneficial or adverse effects of nori consumption is required. KEYWORDS: iron, nori, plant-derived food, Porphyra sp., purple laver, vitamin B12

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cylindrical form and a leaf form of the thallus, respectively.7 The genus Porphyra, including Porphyra tenera and Porphyra yesoensis, is an important marine crop, which is widely cultivated and consumed in Japan, Korea, and China.1 In addition, Porphyra dentata and Porphyra haitanensis are cultivated in Korea and China, respectively.2 Wild Porphyra sp. is also harvested and consumed in these countries. To make a dried nori sheet, raw Porphyra sp. that was harvested from a sea farm is washed with water, cut into small pieces, formed into a sheet (19 cm × 21 cm, dry weight of approximately 3 g) using a nori mat, and dried.1 Dried nori sheets are packaged and are available throughout retail distribution markets. Dried nori sheets become crispy after being toasted or roasted (Figure 1A). The red color of dried nori changes to green during this process because the red pigment phycoerythrin is labile to heat treatment.2,8 Toasted nori sheets and seasoned nori products are commercially prepared at the processing and packaging factories of the nori marketing companies. However, Chinese Porphyra preparation consists of a dried and flattened cake (20−30 cm in diameter) of nori, which is used as an ingredient for flavoring in soups. In Japan, nori is generally used to make sushi or onigiri (rice ball). A large amount of nori can be consumed with certain forms of sushi (vinegared rice rolled with nori). There are also other ways to eat nori, including bread on nori or bread mixed with nori and vegetable soup with nori (Figure 1B). Therefore, dried nori is one of the most commercially available marine products, and the extent of its consumption has been increasing in the recent decades parallel to the popularity of sushi worldwide.

INTRODUCTION The red alga Porphyra sp. is one of the most commercially available marine crop and is well-known as a sea vegetable.1 It is red in color because of the presence of the pigment phycoerythrin,2 which reflects red light and absorbs blue light. This red alga can photosynthesize and live at depths greater than those of most other algae because blue light penetrates water to a greater depth than longer wavelength light. Porphyra sp. also contains green pigment chlorophylls as well as the red pigment.3 Porphyra sp. is mainly farmed in Japan, Korea, and China, and the cultured algal products produce a crop valued at approximately $1.3 billion per year.4 In countries with coastlines along the North Atlantic, such as the United Kingdom, Ireland, Canada, and the United States, wild Porphyra sp. is harvested. Porphyra has various names, being called purple laver (United Kingdom, the United States, and Canada), karengo (New Zealand), nori (Japan), kim (Korea), and zicai (China).5 Dried Porphyra sp. (nori) contains numerous nutrients, including vitamin B12 (B12), and bioactive compounds.4 B12 is the sole vitamin absent from plant-derived food sources.6 Thus, vegetarians are at higher risk of B12 deficiency than nonvegetarians. Our survey of naturally occurring plant-derived food sources with high B12 contents suggested that nori is the most suitable B12 source presently available for vegetarians.6 However, the precise bioavailability of nori B12 in humans is still unclear. The objective of this review is to present up-todate information about the characterization of bioactive compounds of nori that combat various diseases, including B12 deficiency.

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PORPHYRA SPECIES AS EDIBLE ALGAE AND THEIR PRODUCTS Bangiophyceae is composed of five orders, including Bangiales, which in turn contains only one family, Bangiaceae, with two genera, Bangia and Porphyra. Bangia and Porphyra have a © 2017 American Chemical Society

Received: Revised: Accepted: Published: 10685

October 10, 2017 November 20, 2017 November 21, 2017 November 21, 2017 DOI: 10.1021/acs.jafc.7b04688 J. Agric. Food Chem. 2017, 65, 10685−10692

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Journal of Agricultural and Food Chemistry

on a dry basis),10,11 with eicosapentaenoic acid (1200 mg/100 g on a dry basis) and palmitic acid (500 mg/100 g on a dry basis) being the predominant fatty acids in it.11 Eicosapentaenoic acid is an important polyunsaturated fatty acid found in fish oil that reportedly shows potentially beneficial cardiovascular effects as a bioactive mediator.13 These macronutrients of dried nori are identical to those of toasted nori,11 which is one of the most available nori products in Japan. With regard to the vitamin and mineral contents of dried nori, high levels of vitamin K (approximately 2600 μg/100 g on a dry basis), vitamin C (approximately 160 mg/100 g on a dry basis), folate (approximately 1200 μg/100 g on a dry basis), and B12 (approximately 78 μg/100 g on a dry basis) are found in dried nori relative to those in soybean. However, during the toasting of dried nori, the level of vitamin K (approximately 390 μg/100 g on a dry basis) is significantly reduced. Although B12 is the sole vitamin that is absent from plant-derived food sources, dried and toasted nori products (approximately 78 and 58 μg/100 g on a dry basis, respectively) contain a substantial amount of it, with its level being significantly higher in Porphyra sp. than in other edible algae.14,15 A large amount of minerals (approximately 10% on a dry basis) is found in dried nori.11 For example, substantial amounts of potassium (approximately 3100 mg/100 g on a dry basis) and iodine (approximately 1400 μg/100 g on a dry basis) are found in dried and toasted nori products.11 Iron. Although most plant-derived foods are well-known to contain low levels of iron11 and moreover usually contain components that inhibit iron absorption,16 a large amount of iron (approximately 11 mg/100 g on a dry basis) is also found in nori products.11 In this context, the bioavailability of iron from dried nori was determined using a rat hemoglobin regeneration bioassay,17 suggesting that dried nori can be used as a natural iron source in the diet. To study the bioavailability of iron from Porphyra sp., the bioavailability of isotope iron added to Porphyra sp. was estimated in human subjects.18,19 The absorption of iron from rice-based meals was significantly lower with 10 g of raw Porphyra sp. (approximately 6.4%) compared with 20 g of laver (14.9%).18 The effect of the cooking procedure on iron absorption was also evaluated, indicating that the level of iron absorption tended to be higher when subjects consumed cooked algae.18 Using maize and wheat bread containing different concentrations of Porphyra sp., iron bioavailability was measured under the same conditions. The level of absorption of iron from maize and wheat bread was significantly lower with 5 g of raw nori (approximately 12.4 and 15.3%, respectively) compared with 7.5 g of raw nori (approximately 19.4 and 21.8%, respectively).19 These results indicate that Porphyra sp. has a high iron concentration and is a good source of bioavailable iron. Vitamin B12. B12 is usually represented as cyanocobalamin, which is more chemically stable than hydroxocobalamin, methylcobalamin, and 5′-deoxyadenosylcobalamin (Figure 2A). In particular, methylcobalamin is the cofactor of methionine synthase (EC 2.1.1.13), and 5′-deoxyadenosylcobalamin functions as the coenzyme of methylmalonyl-CoA mutase (EC 5.4.99.2).20 In this review, the term B12 refers to cobalamin compounds having B12 activity. Various species of Porphyra are most widely consumed as dried nori sheet products, which contain substantial amounts of B12 (approximately 78 μg/100 g of dry weight) as determined using the Lactobacillus delbrueckii ATCC7830 microbiological method.11 Dried Korean nori reportedly contains 66.8−133.8 μg of B12/

Figure 1. Procedures for making dried and toasted nori products and various ways to eat dried nori products. (A) Raw Porphyra sp. was harvested from a sea farm, washed with water (1), cut into small pieces (2), formed into a sheet (19 cm × 21 cm, dry weight of approximately 3 g) using a nori mat (3), and dried (4). Dried nori sheets can be made crispy by being toasted or roasted (5). (B) (1) Onigiri (rice ball), (2) sushi (vinegared rice rolled with nori), (3) bread on nori, and (4) vegetable soup with nori.

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GENERAL NUTRIENTS OF PORPHYRA SP. (NORI) PRODUCTS Dried nori contains various nutrients, such as proteins, dietary fibers, polyunsaturated fatty acids, minerals, and vitamins,9 and a large amount of proteins (approximately 40% on a dry basis).10,11 This protein content is higher than that of soybeans (dried, raw; approximately 33% on a dry basis).11 Lysine is the first limiting amino acid in dried nori; for dried nori, the amino acid score, which represents the protein quality of this product based on the essential amino acid requirements of humans, is 91,12 indicating that nori protein has excellent nutritional value. A large amount of carbohydrates (approximately 40% on a dry basis) is also found in dried nori,11 and most of them are derived from the soluble dietary fiber porphyran, the physiological functions of which are discussed below. However, dried nori contains a small amount of lipids (approximately 4% 10686

DOI: 10.1021/acs.jafc.7b04688 J. Agric. Food Chem. 2017, 65, 10685−10692

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Figure 2. Structural formula of vitamin B12 and partial structures of vitamin B12-related compounds. (A) (1) 5′-Deoxyadenosylcobalamin, (2) methylcobalamin, (3) hydroxocobalamin, and (4) cyanocobalamin (vitamin B12). (B) (1) Vitamin B12 and (2) pseudovitamin B12.

100 g of dry weight.8 Dried Chinese nori (zicai), dried New Zealand nori (karengo), and canned Welsh nori (laverbread) were found to contain approximately 60.2 and 28.5 μg of B12/ 100 g of dry weight, and 2.8 μg of B12/100 g of wet weight, respectively (our unpublished data). Various types of toasted nori sheet products are commercially available at local retail markets in Japan. The B12 content of these products is reportedly approximately 58 μg of B12/100 g of dry weight.11 These results clearly indicate that dried and toasted nori products contain substantial amounts of B12. To determine whether dried nori contains true B12 or inactive corrinoids, some B12 compounds were purified and characterized.8,21 A B12 compound was purified from Japanese and Korean dried nori products and identified as B12, but not as the corrinoids inactive in humans. Dried nori was found to contain B12 coenzymes (5′-deoxyadenosylcobalamin and methylcobalamin), the contents of which varied from approximately 6 to 90% mainly because of the drying process (dried by exposure to sunlight or a hot wind) and/or storage conditions (storage time, temperature, and humidity).8,21,22 Biochemical and bioinformatics studies indicated that half of all algal species require B12 for their growth.23 P. tenera required B1223 and took up and acquired exogenous B12,24 but it is

unclear whether the growth of all Porphyra species shows B12 dependency. Although various B12-requiring microalgae contained B12-dependent methionine synthase and methylmalonylCoA mutase,25,26 the occurrence and characterization of both B12-dependent enzymes have not been reported in Porphyra sp. Using liquid chromatography−electrospray ionization tandem mass spectrometry analysis, two corrinoids (major, B12; minor, pseudovitamin B12) (Figure 2B) were also detected in Chinese dried nori (unpublished data). Other than B12, pseudovitamin B12 is the only cobamide found most commonly in food.20 In particular, edible cyanobacteria contain a substantial amount of pseudovitamin B12.27 Even if pseudovitamin B12-containing food were ingested, pseudovitamin B12 cannot disturb the gastrointestinal absorption of B12 or the enzymatic reactions of cobalamin-dependent enzymes in mammals.20 Dagnelie et al.28 reported the effect of dried nori on the hematological status of vegans. Although an increase in the plasma B12 concentration in vegans consuming nori (0.1−2.7 μg of B12/day) was indicated, mean corpuscular volume (MCV) values deteriorated further. Rauma et al.29 also reported that vegans consuming nori (approximately 5.0 μg of B12/day) showed serum B12 concentrations higher than those not 10687


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particular, contains large amounts of iron compared with other plant-derived foods. Moreover, eicosapentaenoic acid and B12 are absent in plant-derived food sources. Besides these nutrients, dried nori also contains various biologically active compounds, which reportedly show beneficial effects on mammals, such as anti-inflammatory, antioxidative, and antitumor effects, and improves lipid metabolism.9

consuming it. These results indicate that nori B12 can increase serum B12 levels but fails to improve the hematological index in cases of B12 deficiency. Recently, Schwarz et al.30 reported that when vegans consumed dried nori (P. yezoensis, 106 μg of B12/ 100 g of dry weight, 2.4 μg of B12/day) and sundried wild mushrooms (2.2−8.5 μg of B12/100 g of dry weight, 0.7 μg of B12/day) for 8 months, serum total B12 and MCV levels were normal, serum holotranscobalamin and homocysteine levels were within tolerable levels, but MMA values were elevated. In addition, a nutritional analysis of vegans who had consumed vegan diets including brown rice and dried nori (approximately 2 μg of B12/day) for 4−10 years suggested that the consumption of dried nori prevents B12 deficiency in this group.31 However, Yamada et al.32 demonstrated that, although urinary methylmalonic acid (UMMA) excretion did not change when healthy volunteers (no vegetarians) were given 320 g of raw nori (P. tenera, 40 μg of B12) daily, it increased when volunteers were given 40 g of dried nori (5.8 μg of B12) daily during the test period. In addition, approximately 65% of total B12 found in dried nori is reportedly derived from unidentified B12 analogues. The authors explained this phenomenon as being due to the presence of unidentified B12 compounds (harmful B12 analogues) in dried nori. To clarify the bioavailability of B12 in dried nori (P. yezonensis), the effects of feeding dried nori to B12-deficient rats were investigated.33 When 9-week-old B12-deficient rats, which excreted substantial amounts of UMMA (71.7 ± 20.2 μmol/day), were fed a diet supplemented with dried nori (10 μg/kg diet) for 20 days, UMMA excretion became undetectable and hepatic B12 (especially adenosylcobalamin) levels significantly increased. When the availability of B12 from the other dried nori (P. tenera) was also evaluated in B12-depleted rats, B12 from the dried nori was significantly absorbed by the rats.34 These results indicate that B12 from dried nori is bioavailable to rats. However, it is completely unclear why the MMA level in serum or urine was increased in human subjects consuming dried nori. Although some researchers have speculated that nori contains substantial amounts of harmful B12 analogues that can inhibit cellular B12 metabolism,35 there is no information about the details (chemical properties, chemical structures, inhibition mechanisms, etc.) of such unidentified B12 analogues. The bioavailability of nori B12 in humans remains to be determined in detail. There are two essential factors for evaluating the bioavailability of nori B12 in human studies. (1) The precise B12 content of dried nori samples used in human studies should be determined. Because inactive corrinoids for humans such as pseudovitanim B12 are active in L. delbrueckii ATCC 7830, which is still mainly used to determine the B12 content of food, B12 compounds found in nori samples must be identified using liquid chromatography−electrospray ionization tandem mass spectrometry. (2) A considerably large amount of dried nori samples (>5 μg of B12/day) should be used in feeding experiments. This is because, on the basis of in vitro gastrointestinal digestion experiments, the digestion rate of B12 from dried nori was estimated to be approximately 50%.8 Consumption of a larger amount of nori (approximately 5.0 μg B12/day) significantly increased the serum B12 level of vegans relative to that of vegans consuming a smaller amount of nori (approximately 1.0 μg B12/day).29 These findings indicated that the daily consumption of dried nori would contribute to the intake of essential nutrients, proteins, dietary fibers, eicosapentaenoic acid, vitamin K, vitamin C, folate, B12, potassium, iodine, and iron. Nori, in

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BIOLOGICALLY ACTIVE COMPOUNDS OTHER THAN NUTRIENTS Porphyra sp. contains various biologically active compounds such as polysaccharides, phycobiliproteins, peptides, mycosporine-like amino acids, and phenolic compounds (Figure 3). These bioactive compounds show anti-inflammatory, antioxidative, and antitumor activities, among others.

Figure 3. Summary of biologically active compounds found in nori.

Porphyrans. Porphyrans, sulfated polysaccharides, are the main compounds of Porphyra species (>40% of dry weight),36 and their chemical structures have been studied.37,38 A typical porphyran consists of D-galactose, L-galactose, 3,6-anhydro-Lgalactose, 6-O-methyl-D-galactose, and ester sulfate.32 Feeding on dried nori (P. tenera) powder showed chemopreventive effects against diethylnitrosamine-induced rat hepatocarcinogenesis.39 In human gastric cancer cells, isolated porphyran appears to downregulate insulin-like growth factor-I receptor phosphorylation and then to induce caspase-3 activation to induce the death of cancer cells.40 Moreover, polysaccharides prepared from P. yezoensis considerably inhibited human gastric and lung cancer cell growth, and degradation products of these polysaccharides resulting from an ultrasonic treatment significantly increased this antiproliferative effect against only human gastric cancer cells.41 Porphyra sp. also reportedly contains various anticancer compounds other than porphyrans.42−44 Indeed, in a human case-control study, it was reported that a high rate of intake of nori (Porphyra sp.) may decrease the risk of breast cancer.45 10688


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tigated,67 this compound suppressed the production of reactive oxygen species and increased the levels of extracellular matrix components, procollagen, type I collagen, and elastin.64 In addition, an extract of Porphyra umbilicalis containing porphyra334 and shinorine reduced the level of DNA damage and lipid peroxidation.67 Other Bioactive Compounds. Porphyra sp. also contains the following bioactive compounds, phenolic compounds,68 phlorotannin,69 and taurine.70 Phenolic compounds of P. dentata were identified as catechol, rutin, and hesperidin.68 The P. dentata crude extract containing these phenolic compounds inhibited the production of nitric oxide by stimulating the production of lipopolysaccharide. Other phenolic compounds such as phlorotannins (polymers of phloroglucinol and 1,3,5-trihydroxybenzene) can absorb UV radiation and act as antioxidants and then protect cells against photodamage.69 Phlorotannins reportedly exhibited a protective effect against UV-B-induced skin carcinogenesis71 and inhibited degradation of the skin collagen matrix.72 Taurine, 2-aminoethanesulfonic acid, which is not incorporated into proteins,73 has numerous beneficial effects, such as acting as a neurotransmitter, an antioxidant, a modulator of intracellular calcium levels, and an osmolyte.73 Taurine is present in meat and dairy products, but not in plant-based foods, while seafood is also a good source of this compound (farmed salmon, approximately 60 mg/100 g of wet weight). In particular, dried nori reportedly contains a high level of taurine. Using an ultrasound-assisted extraction method, taurine was extracted from dried nori (P. yezoensis) and determined to be present at a concentration of approximately 13.0 mg/g on a dry basis. Thus, dried nori is available as a taurine-rich plant food. As described above, Porphyra sp. contains various biologically active compounds such as polysaccharides, phycobiliproteins, peptides, mycosporine-like amino acids, and phenolic compounds. These compounds exhibit various pharmacological activities, such as immunomodulation, anticancer, antihyperlipidemic, and antioxidative activities, indicating that consumption of nori is beneficial to human health. Further evidence of such beneficial effects from human studies is required.

The administration of porphyran isolated from P. haitanensis induced the generation of tumor necrosis factor-α and IL-10 in both mice and murine monocyte−macrophage RAW264.7 cells,46 suggesting that P. haitanensis porphyran has immunomodulatory activity. P. haitanensis porphyran also showed antioxidant activity in in vitro experiments.47,48 Moreover, upon the intraperitoneal administration of porphyran to aging mice, the activities of superoxide dismutase and glutathione peroxidase as well as the total antioxidant capacity were increased significantly and the level of lipid peroxidation was significantly decreased,49 suggesting that porphyran has antioxidant activity both in vitro and in vivo. Previously published findings suggest that porphyrans have pharmaceutical properties, such as antitumor,36 antioxidant,43−45 and immunoregulatory activities.50,51 In addition, porphyrans reportedly improved lipid52 and glucose53 metabolism and iron deficiency.54 Phycoerythrin. Porphyra sp. contains two major phycobiliproteins (phycoerythrin and phycocyanin), which act as lightharvesting proteins. Poryphyra sp. has a red color because of the presence of the pigment phycoerythrin, which is composed of phycoerythrobilin (chromophore, a linear tetrapyrole compound) and apoprotein. Phycoerythrin has been reported to have various therapeutic activities such as hepatoprotective, antioxidant,55 anti-aging,56 and anti-inflammatory effects.57 When phycoerythrin is orally ingested during gastrointestinal digestion, it releases the chromophore moiety, phycoerythrobilin. Thus, the therapeutic activities of phycoerythrin in mammals would be due to the formed phycoerythrobilin. Indeed, phycoerythrobilin showed a potent antioxidative activity in in vitro experiments and significantly inhibited the release of β-hexosaminidase in rat basophilic leukemia cells,53 suggesting that phycoerythrobilin exhibits anti-inflammatory activity. Bioactive Peptides. Porphyra sp. contains various bioactive peptides that include PPY, which plays a role in antitumor cell signaling to activate apoptosis,58,59 and ALEGGKSSGGGEATRDPET (known as PY-PE), which exerts a proliferative effect on intestinal epithelial cells.60 Moreover, a hydrolysate of P. yezoensis showed potent inhibitory activity on angiotensin Iconverting enzyme (ACE), which functions as an important negative regulator of the renin−angiotensin system to regulate blood pressure. The oral administration of the ACE inhibitory compounds isolated from P. yezoensis hydrolysate to spontaneously hypertensive rats showed a significant antihypotensive effect.61 The amino acid sequences of Porphyra ACE inhibitory peptides were identified as Ile-Tyr, Met-Lys-Tyr, Ala-Lys-TyrSer-Tyr, and Leu-Arg-Tyr. A dipeptide, anserine (3-methylhistidine), was also identified as an antioxidative compound in P. yezoensis, and its antioxidative activity has been extensively studied. The hydrolysate of Porphyra columbina reportedly has substantial immunomodulatory activity revealed by in vitro experiments, but the peptides involved in this activity have not been identified.62 Mycosporine-like Amino Acids. Mycosporine-like amino acids are ultraviolet-absorbing compounds produced by cyanobacteria, fungi, and marine micro- and macroalgae.63 In particular, porphyra-334 is the most abundant mycosporine-like amino acid in P. yezoensis64 and has been reported to show antioxidant65 and wound-healing66 activities. When the protective effect of porphyra-334 on ultraviolet (UV)-Ainduced photoaging in human skin fibroblasts was inves-

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HARMFUL INGREDIENTS IN PORPHYRA SPECIES Arsenic is one of the most notoriously toxic elements to humans. Inorganic arsenic compounds such as arsenite and arsenate have potent toxic and carcinogenic effects.74 However, organic arsenic compounds such as arsenobetaine and arsenosugars are considered to be nontoxic.75,76 Dried and toasted Chinese nori (Porphyra sp.) products contain 2.1−21.6 mg of total arsenic/kg of dry weight, 0.3−13.9 mg of arseno phosphate sugar/kg of dry weight, and 0.7−6.2 mg of arseno glycerol sugar/kg of dry weight.74 These organic arsenic compounds represent approximately 62% of the total arsenic. Dried nori samples contain no arsenic or a trace amount (approximately 0.1 mg/kg of dry weight) of inorganic arsenic and total arsenic content (approximately 33.8 and 40.1 mg/kg of dry weight, respectively).77,78 Baking treatment (200 °C for 5 min) significantly increased total and inorganic arsenic contents in the soluble fraction (as a bioaccessible fraction) prepared by the in vitro gastrointestinal digestion of nori samples.78 However, similar cooking did not alter the amounts of arsenic compounds in the methanol/water extract of nori.75 It was also found that the arsenosugar bioaccessibility was high (>80%) and did not vary as a result of cooking.79 10689


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After ingestion of dried nori, the concentration of urinary arsenic (mainly dimethylarsenate) immediately increased in humans.74 Recently, thio-dimethylarsinosyacetate, thio-dimethylarsinoyethanol, and thio-dimethylarsenate were identified as urinary arsenic metabolites.80 Cadmium (Cd) is a widespread heavy metal that is toxic to humans. The Cd concentration (0.58−11.0 mg/kg of dry weight) in Porphyra sp. products was reported to vary.81−83 Thus, it is recommended the dried nori products with lower arsenic and Cd contents be chosen for consumption. Edible shrimp and crab are frequently involved in immunoglobulin E-mediated allergies.84,85 Amphipods are concomitantly found in dried nori products at high levels (several milligrams per sheet, 3 g). Thus, the allergenicity and allergens of amphipods (unidentified) found in dried nori sheets were studied.86 Nori amphipods exhibited allergenicity because of an immunoreactive component with a molecular mass of 37 kDa, which was identical to the mass of Japanese spiny lobster tropomyosin.87 These results suggest that amphipods concomitant with dried nori products have the potential to cause serious allergic reactions, particularly in severely sensitized crustacean-allergic patients. These results indicated that dried nori contains such harmful compounds as well as various beneficial compounds. Therefore, daily consumption of a large amount of dried nori products is not recommended, and dried nori products with less harmful ingredients should be chosen for consumption.

This work was supported by JSPS KAKENHI Grant 25450168 (F.W.). Notes

The authors declare no competing financial interest.

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(1) Levine, I. A.; Sahoo, D. In Porphyra: Harvesting Gold from the Sea; I. K. International Publishing House Pvt. Ltd.: New Delhi, 2010. (2) Niu, J. F.; Chen, Z. F.; Wang, G. C.; Zhou, B. C. Purification of phycoerythrin from Porphyra yezoensis Ueda (Bangiales, Rhodophyta) using expanded bed absorption. J. Appl. Phycol. 2010, 22, 25−31. (3) Oh, S.; Shin, M.; Lee, K.; Choe, E. Effects of water activity on pigments in dried laver (Porphyra) during storage. Food Sci. Biotechnol. 2013, 22, 1523−1529. (4) Blouin, N. A.; Brodie, J. A.; Grossman, A. C.; Xu, P.; Brawley, S. H. Porphyra: a marine crop shaped by stress. Trends Plant Sci. 2011, 16, 29−37. (5) Niu, J. F.; Wang, G. C.; Zhou, B. C.; Lin, X. Z.; Chen, C. S. Purification of R-phycoerythrin from Porphyra haitanesis (Bangiales, Rhodophyta) using expanded-bed absorption. J. Phycol. 2007, 43, 1339−1347. (6) Watanabe, F.; Yabuta, Y.; Bito, T.; Teng, F. Vitamin B12containing plant food sources for vegetarians. Nutrients 2014, 6, 1861− 1873. (7) Saga, N. Porphyra: Model plants in marine sciences. In Porphyra yesoensis; Mikami, K., Ed.; Nova Science Publishers, Inc.: Hauppauge, NY, 2012; pp 1−14. (8) Miyamoto, E.; Yabuta, Y.; Kwak, C. S.; Enomoto, T.; Watanabe, F. Characterization of vitamin B12 compounds from Korean purple laver (Porphyra sp.) products. J. Agric. Food Chem. 2009, 57, 2793− 2796. (9) Sugawara, T.; Sakai, S.; Hirata, T. Nutritional and physiological functions of Porphyra. In Porphyra yesoensis; Mikami, K., Ed.; Nova Science Publishers, Inc.: Hauppauge, NY, 2012; pp 181−193. (10) Noda, H. Health benefits and nutritional properties of nori. J. Appl. Phycol. 1993, 5, 255−258. (11) The Council for Science and Technology, Ministry of Education, Culture, Sports, Science and Technology, Japan. Standard Tables of Food Composition in Japan-2010; Official Gazette Cooperation of Japan: Tokyo, 2010. (12) Standard Tables of Food Composition in Japan-2007, 5th Revised and Enlarged Edition; Kagawa Nutrition University Publishing Division: Tokyo, 2006. (13) Brinton, E.; Mason, P. Prescription omega-3 fatty acid products containing highly purified eicosapentaenoic acid (EPA). Lipids Health Dis. 2017, 16, 23. (14) Van den Berg, H.; Dagnelie, P. C.; van Staveren, W. A. Vitamin B12 and seaweed. Lancet 1988, 331, 242−243. (15) Watanabe, F.; Takenaka, S.; Kittaka-Katsura, H.; Ebara, S.; Miyamoto, E. Characterization and bioavailability of vitamin B12compounds from edible algae. J. Nutr. Sci. Vitaminol. 2002, 48, 325− 331. (16) Hallberg, L. Bioavailability of dietary iron in man. Annu. Rev. Nutr. 1981, 1, 123−147. (17) Shaw, N.-S.; Liu, Y.-H. Bioavailability of iron from purple laver (Porphyra spp.) estimated in a rat hemoglobin regeneration bioassay. J. Agric. Food Chem. 2000, 48, 1734−1737. (18) García-Casal, M. N.; Pereira, A. C.; Leets, I.; Ramírez, J.; Quiroga, M. F. High iron content and bioavailability in humans from four species of marine algae. J. Nutr. 2007, 137, 2691−2695. (19) García-Casal, M. N.; Ramírez, J.; Leets, I.; Pereira, A. C.; Quiroga, M. F. Antioxidant capacity, polyphenol content and iron bioavailability from algae (Ulva sp., Sargassum sp. and Porphyra sp.) in human subjects. Br. J. Nutr. 2009, 101, 79−85. (20) Watanabe, F.; Bito, T. Corrinoids in food and biological samples. In Frontiers in Natural Product Chemistry; Atta-ur-Rahman,

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CONCLUDING REMARKS This review indicates that dried nori (Porphyra sp.) contains various kinds of biologically active compounds and essential nutrients, the levels of some of which (iron, B12, and eicosapentaenoic acid) are higher than in most plant-derived foods. Indeed, such nutrients are significantly lacking in the diets of vegetarians. The consumption of dried nori products would provide human health benefits, especially for vegetarians. Although many analytical studies have indicated that dried and toasted nori products contain substantial amounts of B12, it still remains possibile that nori B12 is destroyed and/or converted into inactive B12 analogues during the drying process and storage. Thus, we stress that, if nori products are to be consumed as a sole B12 source, B12 compounds found in nori products must be determined and identified precisely. Moreover, a high rate of intake of nori products indicated a decrease in the risk of breast cancer in humans,45 but Porphyra sp. reportedly contains toxic metals (arsenic and Cd) and/or amphipod allergens, the levels of which vary significantly among nori products. Thus, dried nori products with less harmful ingredients should be chosen for consumption. Further evidence of the beneficial effects of nori due to the nutrients and bioactive compounds from human studies is required.

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REFERENCES

AUTHOR INFORMATION

Corresponding Author

*Phone and fax: +81-857-31-5412. E-mail: watanabe@muses. tottori-u.ac.jp. ORCID

Fumio Watanabe: 0000-0001-6654-4148 Author Contributions

All authors contributed equally to the preparation of the manuscript and have approved the final version. 10690


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Bioactive Compounds of Edible Purple Laver Porphyra sp. (Nori)

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